Coordination Between Compound-Specific Chemistry and Morphology in Plant Roots Aligns with Ancestral Mycorrhizal Affinity in Temperate Angiosperms

Abstract:

Foliar tissues exhibit trait coordination along an economic spectrum from short-lifespan, acquisitive to long-life span, stress-tolerant strategies, globally. However, such trait coordination has proven elusive in plant roots. With few alternative hypotheses proposed so far, this uncertainty largely challenges our understanding of the adaptation and strategies at the whole-plant level. Different selective pressures that dominate below-ground may render root traits to organize in a unique way that cannot be deduced from the framework of leaves. As roots form fungal symbiosis to facilitate resource acquisition and are continuously exposed to an enormous number of soil microorganisms, the secondary compounds that regulate these biotic interactions could be the key to understanding the functional trade-offs that structure root trait diversity.

Here, for the first time we extend functional trade-offs to molecular-level composition of roots and present a unique dataset covering root compound-specific chemistry, morphology, anatomy, and mycorrhizal status in temperate trees spanning major angiosperm lineages. Our data showed significant phylogenetic structuring in root chemical composition and revealed undocumented coordination between root chemical composition, morphology, and anatomy that contradicts current concepts of plant resource economics derived solely from foliage. Rather, the observed coordination aligns with root trait trade-offs between mycorrhizal affinity and chemical protection, and reflects divergent root strategies that cluster in different evolutionary lineages. Because many secondary protective compounds (e.g., lignin, condensed tannins) influence ecosystem carbon and nitrogen cycling, this work for the first time provide a direct link between root ecological strategies and litter recalcitrance that has significant consequence on biogeochemical process at ecosystem levels. Our study, by linking plant evolutionary history, root ecological strategy, and plant-microbe interactions with compound-specific chemistry, provides novel insights into factors that drive below-ground adaptations in plants, which have implications not only for plant diversity, but also for the further link between plant diversity and soil carbon transformation.